Adiponectin Ameliorates Hyperglycemia-Induced Retinal Endothelial Dysfunction, Highlighting Pathways, Regulators, and Networks

References

• Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376(9735):124–136. doi:10.1016/S0140-6736(09)62124-3
   PubMed Web of Science ®Google Scholar
• Roy S, Kern TS, Song B, Stuebe C. Mechanistic insights into pathological changes in the diabetic retina: implications for targeting diabetic retinopathy. Am J Pathol. 2017;187(1):9–19. doi:10.1016/j.ajpath.2016.08.022
   PubMed Web of Science ®Google Scholar
• Ola MS, Nawaz MI, Siddiquei MM, Al-Amro S, Abu El-Asrar AM. Recent advances in understanding the biochemical and molecular mechanism of diabetic retinopathy. J Diabetes Complications. 2012;26(1):56–64. doi:10.1016/j.jdiacomp.2011.11.004
   PubMed Web of Science ®Google Scholar
• Semeraro F, Cancarini A, dell’Omo R, Rezzola S, Romano MR, Costagliola C. Diabetic retinopathy: vascular and inflammatory disease. J Diabetes Res. 2015;2015:582060. doi:10.1155/2015/582060
   PubMed Web of Science ®Google Scholar
• Rosman N, Froemming G, Effat O, Nawawi H, Singh H. Effects of adiponectin on markers of endothelial activation and markers of inflammation in human coronary artery endothelial cells. J Fundam Appl Sci. 2017;9(6S):1102–1115. doi:10.4314/jfas.v9i6s.81
   Google Scholar
• Yamauchi T, Kamon J, Ito Y, et al. Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature. 2003;423(6941):762–769. doi:10.1038/nature01705
   PubMed Web of Science ®Google Scholar
• Ohashi K, Ouchi N, Matsuzawa Y. Anti-inflammatory and anti-atherogenic properties of adiponectin. Biochimie. 2012;94(10):2137–2142. doi:10.1016/j.biochi.2012.06.008
   PubMed Web of Science ®Google Scholar
• Brakenhielm E, Veitonmaki N, Cao R, et al. Adiponectin-induced antiangiogenesis and antitumor activity involve caspase-mediated endothelial cell apoptosis. Proc Natl Acad Sci U S A. 2004;101(8):2476–2481. doi:10.1073/pnas.0308671100
   PubMed Web of Science ®Google Scholar
• Ouchi N, Kobayashi H, Kihara S, et al. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem. 2004;279(2):1304–1309. doi:10.1074/jbc.M310389200
   PubMed Web of Science ®Google Scholar
• Fu Z, Gong Y, Lofqvist C, Hellstrom A, Smith LE. Review: adiponectin in retinopathy. Biochim Biophys Acta. 2016;1862(8):1392–1400. doi:10.1016/j.bbadis.2016.05.002
   PubMed Web of Science ®Google Scholar
• Klaassen I, de Vries EW, Vogels IMC, et al. Identification of proteins associated with clinical and pathological features of proliferative diabetic retinopathy in vitreous and fibrovascular membranes. PLoS One. 2017;12(11):e0187304–e0187304. doi:10.1371/journal.pone.0187304
   PubMed Web of Science ®Google Scholar
• Ucgun NI, Zeki-Fikret C, Yildirim Z. Inflammation, and diabetic retinopathy. Mol Vis. 2020;26:718–721.
   PubMed Web of Science ®Google Scholar
• Yilmaz MI, Sonmez A, Acikel C, et al. Adiponectin may play a part in the pathogenesis of diabetic retinopathy. Eur J Endocrinol. 2004;151(1):135–140. doi:10.1530/eje.0.1510135
   PubMed Web of Science ®Google Scholar
• Yang HS, Choi YJ, Han HY, et al. Serum, and aqueous humor adiponectin levels correlate with diabetic retinopathy development and progression. PLoS One. 2021;16(11):e0259683. doi:10.1371/journal.pone.0259683
   PubMed Web of Science ®Google Scholar
• Tien T, Zhang J, Muto T, Kim D, Sarthy VP, Roy S. High glucose induces mitochondrial dysfunction in retinal Muller cells: implications for diabetic retinopathy. Invest Ophthalmol Vis Sci. 2017;58(7):2915–2921. doi:10.1167/iovs.16-21355
   PubMed Web of Science ®Google Scholar
• Rizk NM, Fadel A, AlShammari W, Younes N, Bashah M. The immunophenotyping changes of peripheral CD4+ T lymphocytes and inflammatory markers of class III obesity subjects after laparoscopic gastric sleeve surgery - A follow-up study. J Inflamm Res. 2021;14:1743–1757.
   PubMed Web of Science ®Google Scholar
• Sharma I, Rizk N, Falel AS, Al-Shabrawey MA-S. Docosahexaenoic acid (DHA)-a novel therapeutic intervention for mitigating hypoxia induced retinal endothelial dysfunction. Invest Ophthalmol Vis Sci. 2015;56(7):21.
   Web of Science ®Google Scholar
• Srinivasan V, Sulochana KN. Effect of adiponectin on expression of vascular endothelial growth factor and pigment epithelium-derived factor: an in vitro study. Indian J Pharmacol. 2015;47(1):117–120. doi:10.4103/0253-7613.150376
   PubMed Web of Science ®Google Scholar
• Palanisamy K, Nareshkumar RN, Sivagurunathan S, Raman R, Sulochana KN, Chidambaram S. Anti-angiogenic effect of adiponectin in human primary microvascular and macrovascular endothelial cells. Microvasc Res. 2019;122:136–145. doi:10.1016/j.mvr.2018.08.002
   PubMed Web of Science ®Google Scholar
• Ding G, Qin Q, He N, et al. Adiponectin and its receptors are expressed in adult ventricular cardiomyocytes and upregulated by activation of peroxisome proliferator-activated receptor gamma. J Mol Cell Cardiol. 2007;43(1):73–84. doi:10.1016/j.yjmcc.2007.04.014
   PubMed Web of Science ®Google Scholar
• Lin T, Qiu Y, Liu Y, Mohan R, Li Q, Lei B. Expression of adiponectin and its receptors in type 1 diabetes mellitus in human and mouse retinas. Mol Vis. 2013;2013(19):1769–1778.
   Google Scholar
• Ouedraogo R, Wu X, Xu SQ, et al. Adiponectin suppression of high-glucose-induced reactive oxygen species in vascular endothelial cells: evidence for involvement of a cAMP signaling pathway. Diabetes. 2006;55(6):1840–1846. doi:10.2337/db05-1174
   PubMed Web of Science ®Google Scholar
• Singh LP. Thioredoxin Interacting Protein (TXNIP) and Pathogenesis of Diabetic Retinopathy. J Clin Exp Ophthalmol. 2013;2013:4.
   Google Scholar
• Mossalam M, Jeong JH, Abel ED, Kim SW, Kim YH. Reversal of oxidative stress in endothelial cells by controlled release of adiponectin. J Control Release. 2008;130(3):234–237. doi:10.1016/j.jconrel.2008.06.009
   PubMed Web of Science ®Google Scholar
• Xiao X, Dong Y, Zhong J, et al. Adiponectin protects endothelial cells from the damages induced by the intermittent high level of glucose. Endocrine. 2011;40(3):386–393. doi:10.1007/s12020-011-9531-9
   PubMed Web of Science ®Google Scholar
• Akifusa S, Kamio N, Shimazaki Y, Yamaguchi N, Yamashita Y. Regulation of globular adiponectin-induced apoptosis by reactive oxygen/nitrogen species in RAW264 macrophages. Free Radic Biol Med. 2008;45(9):1326–1339. doi:10.1016/j.freeradbiomed.2008.08.005
   PubMed Web of Science ®Google Scholar
• Wang F-P, Li L, Li J, Wang J-Y, Wang L-Y, Jiang W. High mobility group box-1 promotes the proliferation and migration of hepatic stellate cells via TLR4-dependent signal pathways of PI3K/Akt and JNK. PLoS One. 2013;8(5):e64373. doi:10.1371/journal.pone.0064373
   PubMed Web of Science ®Google Scholar
• Baptista FI, Aveleira CA, Castilho AF, Ambrosio AF. Elevated Glucose and Interleukin-1beta differentially affect retinal microglial cell proliferation. Mediators Inflamm. 2017;2017:4316316. doi:10.1155/2017/4316316
   PubMed Web of Science ®Google Scholar
• Ouedraogo R, Gong Y, Berzins B, et al. Adiponectin deficiency increases leukocyte-endothelium interactions via upregulation of endothelial cell adhesion molecules in vivo. J Clin Invest. 2007;117(6):1718–1726. doi:10.1172/JCI29623
   PubMed Web of Science ®Google Scholar
• Chandrasekar B, Boylston WH, Venkatachalam K, Webster NJ, Prabhu SD, Valente AJ. Adiponectin blocks interleukin-18-mediated endothelial cell death via APPL1-dependent AMP-activated protein kinase (AMPK) activation and IKK/NF-kappaB/PTEN suppression. J Biol Chem. 2008;283(36):24889–24898. doi:10.1074/jbc.M804236200
   PubMed Web of Science ®Google Scholar
• Friedlander M, Brooks PC, Shaffer RW, Kincaid CM, Varner JA, Cheresh DA. Definition of two angiogenic pathways by distinct αv integrins. Science. 1995;270(5241):1500–1502. doi:10.1126/science.270.5241.1500
   PubMed Web of Science ®Google Scholar
• Gong H, Zuliani P, Komuravelli A, Faeder JR, Clarke EM. Analysis and verification of the HMGB1 signaling pathway. BMC Bioinform. 2010;11(7):S10. doi:10.1186/1471-2105-11-S7-S10
   PubMed Web of Science ®Google Scholar
• Nebbioso M, Lambiase A, Armentano M, et al. The complex relationship between diabetic retinopathy and high-mobility group box: a review of molecular pathways and therapeutic strategies. Antioxidants. 2020;9(8):666. doi:10.3390/antiox9080666
   Web of Science ®Google Scholar
• Mohammad G, Alam K, Nawaz MI, Siddiquei MM, Mousa A, El-Asrar AMA. Mutual enhancement between high-mobility group box-1 and NADPH oxidase-derived reactive oxygen species mediates diabetes-induced upregulation of retinal apoptotic markers. J Physiol Biochem. 2015;71(3):359–372. doi:10.1007/s13105-015-0416-x
   PubMed Web of Science ®Google Scholar
• Santos ARC, Dvoriantchikova G, Li Y, et al. Cellular mechanisms of high mobility group 1 (HMGB-1) protein action in the diabetic retinopathy. PLoS One. 2014;9(1):e87574. doi:10.1371/journal.pone.0087574
   PubMed Web of Science ®Google Scholar
• Elfeky M, Yoneshiro T, Okamatsu-Ogura Y, Kimura K. Adiponectin suppression of late inflammatory mediator, HMGB1-induced cytokine expression in RAW264 macrophage cells. J Biochem. 2018;163(2):143–153. doi:10.1093/jb/mvx069
   PubMed Web of Science ®Google Scholar
• Cuenda A, Rousseau S. p38 MAP-Kinases pathway regulation, function and role in human diseases. Mol Cell Res. 2007;1773(8):1358–1375.
   PubMed Web of Science ®Google Scholar
• Chan L-P, Liu C, Chiang F-Y, et al. IL-8 promotes inflammatory mediators and stimulates activation of p38 MAPK/ERK-NF-κB pathway and reduction of JNK in HNSCC. Oncotarget. 2017;8(34):56375–56388. doi:10.18632/oncotarget.16914
   PubMedGoogle Scholar
• O’Brown ZK, Van Nostrand EL, Higgins JP, Kim SK, Copenhaver GP. The inflammatory transcription factors NFκB, STAT1 and STAT3 drive age-associated transcriptional changes in the human kidney. PLoS Genet. 2015;11(12):e1005734. doi:10.1371/journal.pgen.1005734
   PubMed Web of Science ®Google Scholar
• Chen Y, Wang J, Li J, et al. Activating transcription factor 4 mediates hyperglycaemia-induced endothelial inflammation and retinal vascular leakage through activation of STAT3 in a mouse model of type 1 diabetes. Diabetologia. 2012;55(9):2533–2545. doi:10.1007/s00125-012-2594-1
   PubMed Web of Science ®Google Scholar
• Sun H, Zhang Y, Gao P, et al. Adiponectin reduces C-reactive protein expression and downregulates STAT3 phosphorylation induced by IL-6 in HepG2 cells. Mol Cell Biochem. 2011;347(1):183–189. doi:10.1007/s11010-010-0627-y
   PubMed Web of Science ®Google Scholar
• Yuuki T, Kanda T, Kimura Y, et al. Inflammatory cytokines in vitreous fluid and serum of patients with diabetic vitreoretinopathy. J Diabetes Complications. 2001;15(5):257–259. doi:10.1016/S1056-8727(01)00155-6
   PubMed Web of Science ®Google Scholar
• Cardinez C, Miraghazadeh B, Tanita K, et al. Gain-of-function IKBKB mutation causes human combined immune deficiency. J Exp Med. 2018;215(11):2715–2724. doi:10.1084/jem.20180639
   PubMed Web of Science ®Google Scholar
• Wu X, Mahadev K, Fuchsel L, Ouedraogo R, Xu SQ, Goldstein BJ. Adiponectin suppresses IkappaB kinase activation induced by tumor necrosis factor-alpha or high glucose in endothelial cells: role of cAMP and AMP kinase signaling. Am J Physiol Endocrinol Metab. 2007;293(6):E1836–E1844. doi:10.1152/ajpendo.00115.2007
   PubMed Web of Science ®Google Scholar
• Sugimoto M, Cutler A, Shen B, et al. Inhibition of EGF signaling protects the diabetic retina from insulin-induced vascular leakage. Am J Pathol. 2013;183(3):987–995. doi:10.1016/j.ajpath.2013.05.017
   PubMed Web of Science ®Google Scholar
• Yamamoto Y, Yamamoto H. Receptor for advanced glycation end‐products‐mediated inflammation and diabetic vascular complications. J Diabetes Investig. 2011;2(3):155. doi:10.1111/j.2040-1124.2011.00125.x
   PubMed Web of Science ®Google Scholar
• Mao X, Kikani CK, Riojas RA, et al. APPL1 binds to adiponectin receptors and mediates adiponectin signaling and function. Nat Cell Biol. 2006;8(5):516–523. doi:10.1038/ncb1404
   PubMed Web of Science ®Google Scholar
• Howell SJ, Lee CA, Batoki JC, et al. Retinal inflammation, oxidative stress, and vascular impairment is ablated in diabetic mice receiving XMD8-92 treatment. Front Pharmacol. 2021;12:732630. doi:10.3389/fphar.2021.732630
   PubMed Web of Science ®Google Scholar
• Chen Q, Qiu F, Zhou K, et al. Pathogenic role of microRNA-21 in diabetic retinopathy through downregulation of PPARα. Diabetes. 2017;66(6):1671–1682. doi:10.2337/db16-1246
   PubMed Web of Science ®Google Scholar
• Santovito D, De Nardis V, Marcantonio P, et al. Plasma exosome microRNA profiling unravels a new potential modulator of adiponectin pathway in diabetes: effect of glycemic control. J Clin Endocrinol Metab. 2014;99(9):E1681–E1685. doi:10.1210/jc.2013-3843
   PubMed Web of Science ®Google Scholar
• Jiang C, Qin B, Liu G, et al. MicroRNA-184 promotes differentiation of the retinal pigment epithelium by targeting the AKT2/mTOR signaling pathway. Oncotarget. 2016;7(32):52340. doi:10.18632/oncotarget.10566
   PubMedGoogle Scholar
• Subedi A, Park P-H. Autocrine and paracrine modulation of microRNA-155 expression by globular adiponectin in RAW 264.7 macrophages: involvement of MAPK/NF-κB pathway. Cytokine. 2013;64(3):638–641. doi:10.1016/j.cyto.2013.09.011
   PubMed Web of Science ®Google Scholar
• Ye E-A, Liu L, Jiang Y, et al. miR-15a/16 reduces retinal leukostasis through decreased pro-inflammatory signaling. J Neuroinflammation. 2016;13(1):305. doi:10.1186/s12974-016-0771-8
   PubMed Web of Science ®Google Scholar
• Zhang L-Q, Cui H, Yu Y-B, Shi H-Q, Zhou Y, Liu M-J. MicroRNA-141-3p inhibits retinal neovascularization and retinal ganglion cell apoptosis in glaucoma mice through the inactivation of docking protein 5-dependent mitogen-activated protein kinase signaling pathway. J Cell Physiol. 2019;234(6):8873–8887. doi:10.1002/jcp.27549
   PubMed Web of Science ®Google Scholar
• Li EH, Huang QZ, Li GC, Xiang ZY, Zhang X. Effects of miRNA-200b on the development of diabetic retinopathy by targeting VEGFA gene. Biosci Rep. 2017;37(2). doi:10.1042/BSR20160572
   Web of Science ®Google Scholar
• Higuchi A, Ohashi K, Kihara S, Walsh K, Ouchi N. Adiponectin suppresses pathological microvessel formation in retina through modulation of tumor necrosis factor-α expression. Circ Res. 2009;104(9):1058–1065. doi:10.1161/CIRCRESAHA.109.194506
   PubMed Web of Science ®Google Scholar
• Dagher Z, Gerhardinger C, Vaz J, Goodridge M, Tecilazich F, Lorenzi M. The increased transforming growth factor-β signaling induced by diabetes protects retinal vessels. Am J Pathol. 2017;187(3):627–638. doi:10.1016/j.ajpath.2016.11.007
   PubMed Web of Science ®Google Scholar
• Tomita Y, Lee D, Tsubota K, Kurihara T. PPARα agonist oral therapy in diabetic retinopathy. Biomedicines. 2020;8(10):433. doi:10.3390/biomedicines8100433
   PubMed Web of Science ®Google Scholar
• Ouchi N, Ohishi M, Kihara S, et al. Association of hypoadiponectinemia with impaired vasoreactivity. Hypertension. 2003;42(3):231–234. doi:10.1161/01.HYP.0000083488.67550.B8
   PubMed Web of Science ®Google Scholar
• Teoh H, Quan A, Bang KW, et al. Adiponectin deficiency promotes endothelial activation and profoundly exacerbates sepsis-related mortality. Am J Physiol Endocrinol Metab. 2008;295(3):E658–E664. doi:10.1152/ajpendo.90384.2008
   PubMed Web of Science ®Google Scholar